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Vol. 14: 127–134, 2011 ENDANGERED SPECIES RESEARCH Published online June 22 doi: 10.3354/esr00350 Endang Species Res Application of the precautionary principle to taxa of uncertain status: the case of the Bellinger River turtle Arthur Georges1,*, Ricky-John Spencer1, 2, Michael Welsh3, H. Bradley Shaffer4, Rachael Walsh1, Xiuwen Zhang1 1Institute for Applied Ecology, University of Canberra, ACT 2601, Australia 2Native and Pest Animal Unit, School of Natural Sciences, University of Western Sydney, Locked Bag 1797, Penrith South, New South Wales 2750, Australia 3Michael Welsh Fauna Consultant, 7 Chisholm Road, Gerringong, New South Wales 2534, Australia 4Department of Evolution and Ecology, University of California, One Shields Ave, Davis, California 95616, USA ABSTRACT: Legislative and regulatory frameworks for conserving biodiversity often focus on the species as a fundamental unit for protection. In cases where the taxonomic or conservation status of a species is uncertain, the precautionary principle may be invoked in listing suspected but as yet undescribed taxa as vulnerable or endangered. In this paper, we present an evaluation of the taxonomic status of what has been regarded as a distinctive but as yet undescribed species of freshwater turtle, declared endangered in the Action Plan for Australian Reptiles and vulnerable in the schedules of state and federal conservation acts. Using mitochondrial sequence variation, we show that the Bellinger River turtle is an unremarkable population of a common and widespread species, Emydura macquarii. In addition, we present evidence suggesting that it may have been recently introduced to, or may be a recent invader of, the Bellinger River (New South Wales, Australia) where it may come to compete with Myuchelys georgesi, an endemic found only in the Bellinger River. Our study illus- trates the need to couple fundamental research with on-ground action early in an adaptive management context, particularly where taxonomic status of the target species is uncertain. Short-term cost savings of failing to do so may come to be greatly exceeded by longer-term opportunity loss where conservation dollars are limited. KEY WORDS: Taxonomic impediment · Emydura macquarii · Myuchelys georgesi · Elseya · Mitochondrial sequence variation Resale or republication not permitted without written consent of the publisher INTRODUCTION Biodiversity encapsulates diversity of biotic communities, diversity of species in those communities, Biodiversity loss is one of the greatest challenges of genetic diversity within species, and the ecological and the 21st century (McGlothlin 2004). Changes brought evolutionary processes that create and maintain that about by growth of human populations and per capita diversity (Wilson & Peter 1988, World Resources Insti- consumption are driving many changes, with adverse tute 1992, de Long 1996). However, in many legislative consequences for wildlife on all continents, through and regulatory systems, the species remains the pri- the combined influences of over-exploitation (Lauck et mary focus for conservation (Hey et al. 2003). As new al. 1998, Rosenberg 2003), deforestation, habitat species are discovered, rapid assessment of their status degradation, fragmentation or loss (Fahrig 1997, becomes a priority so that measures can be taken to Yamaura et al. 2011), exotic predators and diseases ensure that they are protected (Pauly et al. 2007). In (Berger et al. 1998, Daszak et al. 1999, Lips et al. 2006) some jurisdictions, such as Australia, the precautionary and climate change (Walther et al. 2002). principle (Raffensperger et al. 1999) is used to allow *Email: [email protected] © Inter-Research 2011 · www.int-res.com 128 Endang Species Res 14: 127–134, 2011 protection and remediation to be initiated in advance Bellinger River Emydura and use mitochondrial DNA of formal description of ‘species’ thought to be at risk. sequences of Emydura spp. and the endemic Bellinger The Australian Environmental Protection and Biodi- River sawshell turtle Myuchelys georgesi to address versity Conservation (EPBC) Act and most state juris- these 2 questions. Taxonomic research is in decline dictions allow nomination of populations regarded as, despite the biodiversity imperative (Hopkins & Freck- or suspected to be, distinct species or subspecies, some leton 2002), and in Australia is compounded by the of which await formal description. This practice leads proliferation of names attached to taxonomic concepts to satisfactory conservation outcomes when the need with little or no support (see Georges & Thomson 2010, for management intervention is pressing, but the infor- Oliver & Lee 2010) and uncritically adopted by state mation needed to make sound taxonomic judgements and federal agencies. The role of a well-founded tax- has yet to be fully realised. The risk is that conserva- onomy in underpinning conservation is well estab- tion resources may be allocated on taxa that later turn lished (Mace 2004). Our study serves to highlight the out to be of relatively low conservation value (Zhu et importance of a commitment to fundamental taxo- al. 1998). Such would occur when the initial judgement nomic research, concurrent with the early stages of on the validity of a taxon is not borne out by sub - precautionary management intervention, to address sequent investigation. the uncertainty in knowledge that leads to the invoca- Here we present an example where the precaution- tion of the precautionary principle in the listing of new ary principle was applied to what was, on the basis of taxa whose taxonomic status is uncertain. anecdotal evidence, a ‘species’ at risk — a distinctive form of freshwater turtle found only in the Bellinger River of eastern Australia (Cann 1998). Listed as vul- MATERIALS AND METHODS nerable in the Reptile Action Plan (Cogger et al. 1993) as Emydura signata, vulnerable in the Schedules of the Turtles were collected between 1 and 17 April 2007 Threatened Species Act, New South Wales (NSW in the Bellinger and Kalang Rivers (New South Wales, NPWS 2001) as E. macquarii, Bellinger River Form, Australia) (Fig. 1) by hand with mask and fins, in and vulnerable in the national EPBC Act (Common- cathedral traps (Legler 1960, as modified by Georges wealth of Australia 1999) as E. macquarii signata et al. 2006) baited with liver and sardines, and with (Bellinger River, NSW), this ‘species’ of turtle was used dipnets by spotlight at night. Traps were checked at as a flagship to marshal community support for a range intervals of 4 to 10 h, re-baited after approximately of initiatives in riparian and riverine restoration and 24 h, and left in place for 24 to 48 h at each location. invasive fox control (NSW NPWS 2001). Discovered in Mature males were distinguished from mature fe- 1990 in a single waterhole in the middle reaches of the males based on tail length (Georges et al. 2006), and the Bellinger River by P. King (King & Heatwole 1994) as minimum size of visually identifiable males (118 mm part of broader studies and again at the same location carapace length) was used as the upper size limit for all in 1992 by Cann (1998), captures of the Bellinger Emy- juveniles. A small sliver of tissue was taken from the out- dura were initially ex tremely rare. Recent surveys side edge of the vestigial toe of the rear foot, stored in funded by the NSW Government have shown progres- 75% ethanol for DNA analysis, and later transferred to sive increases in abundance and distribution in the –20°C storage freezers. Each turtle was photographed Bellinger River, to the point where the turtles are now (dorsal and ventral view, lateral view of the head) and widespread and common in the drainage. However, presence or absence of the cervical scute and/or head the question of whether the Bellinger River Emydura is shield was noted, characters which ty pically differ be- a distinctive taxon or an unremarkable representative tween Emydura macquarii and Myu chelys georgesi. All of the more widespread E. macquarii macquarii (sensu turtles were released within 2 h at their point of capture. Georges & Thomson 2010) remains unanswered. So DNA was extracted from the 76 specimens of Emy- too does the more difficult question of whether it is a dura macquarii, 16 Myuchelys georgesi, 3 suspected relict endemic having barely endured and recovered hybrids and 1 suspected specimen of M. latisternum from a catastrophic decline, or whether it is a recent from the Bellinger River drainage (including the introduction to the river, possibly with human assis- Kalang tributary). An additional 34 specimens of E. tance, that has established and is in the early stages of macquarii from 3 localities in the vicinity of Coffs Har- invasion. Both questions are critical to deciding what bour were also extracted as a second phase in the management intervention is required, if any, and the study. Genomic DNA was extracted from skin tissues value of the Bellinger River Emydura as a flagship using salt extraction or Chelex (Bio-Rad) beads as species of conservation concern. described by FitzSimmons et al. (1997). Sub-samples of In this paper, we report the results of the most recent skin were digested overnight at 55°C in 300 µl of buffer survey into the distribution and abundance of the (40 mM Tris, 20 mmol EDTA, 100 mmol NaCl), 20 µl of Georges et al.: Precautionary principle and undescribed taxa 129 Fig. 1. Bellinger catchment (at the junction of the crosshairs in the inset) showing the capture localities of the Bellinger Emydura (d). The Kalang River is essentially a tributary of the Bellinger River, and is shown on the map as running through Urunga and Brierfield (lighter shading) 10% sodium dodecyl sulphate (SDS) and 10 µl of 10 mg and 4 bp (Table 1). In contrast, the endemic Myuchelys ml–1 Proteinase K. DNA was salt extracted and precip- georgesi yielded only a single haplotype (Genbank itated with 150 µl of 7.5 mol ammonium acetate and 1 accession nos.

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